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UC Irvine UC Irvine Previously Published Works UC Irvine UC Irvine Previously Published Works Title Histocompatibility bioassays of population structure in marine sponges: Clonal structure in verongia longissima and lotrochota birotulata Permalink https://escholarship.org/uc/item/0g93w1qg Journal Journal of Heredity, 74(3) ISSN 0022-1503 Authors Neigel, JE Avise, JC Publication Date 1983 DOI 10.1093/oxfordjournals.jhered.a109750 License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California The Journal of Heredity 74: 134-140. 1983. Histocompatibility bioassays of population structure in marine sponges Clonal structure in Verongia longissima and lotrochota birotulata ABSTRACT: Clonal population structure In two marine sponges, Verongia longissima and lotrochota birotulata, was examined with a self-recognition bioassay. The bloassay con- sists of grafts of branch segments between conspecific individuals. Results were consis- tent with the operational properties expected of a precise histocompatibility system. Auto- grafts exhibited acceptance responses; grafts between individuals separated by large dis- tances exhibited rejection responses; individuals were not limited to a single mode of re- sponse at one time; and all identity relationships were transitive. Clonal population struc- ture was assessed by examining the relationship between graft response and donor-to- reclplent distance, and by actually mapping the distributions of particular clones. Clones Joseph E. Neigel of lotrochota birotulata were usually restricted to single coral heads or small patch reefs (1-3 m diameter). For Verongia longissima, which can grow directly upon the coral rubble John C. Avise surrounding coral heads and patch reefs, individual clones often occupied larger areas (up to 10 m diameter). The spatial patterns of clonal distributions are readily interpreted as consequences of the particular demographies and habitat specificities of these two species. THE SPATIAL distribution of asexual linea- ena as bioassays of clonal population structure ges or clones is an important component of has been demonstrated with self-incompati- genetic structure in the populations of many bility in clover and grasses12"14, histocompa- plants and sedentary invertebrates. The tibility in parthenogenetic vertebratesl-6-28, preservation of characteristic genotypes by and interclonal aggression in sea anemones35. clonal propagation implies that clonal struc- Of potentially much wider application, how- ture can be resolved by any method that assays ever, are invertebrate "histocompatibility" a sufficiently polymorphic subset of the ge- systems, which recently have been demon- nome. Polymorphic allozyme and morpho- strated in several major phyla5'19-20^2'24'25. If logical markers have been thus employed to invertebrate histocompatibility systems prove identify clones within natural popula- to be generally capable of resolving genetic tions 17,21,31.32,36,37 However, another class of variation in natural populations, they will then genetic markers is perhaps ideally suited for constitute a powerful tool for analysis of pop- the analysis of clonal population structure: ulation structure in a large and diverse group those manifested in various self-recognition of organisms. The authors arc, respectively, graduate student and phenomena. associate professor in the Department of Molecular and From what is already known of invertebrate Population Genetics, the University of Georgia, Athens, Self-recognition phenomena, such as self- histocompatibility systems and histocompa- GA 30602. They wish to thank the University of the incompatibility in flowering plants, and his- tibility systems in general, it is apparent that West Indies' Discovery Bay Marine Laboratory in Ja- not all responses in contacts between conspe- maica for their cooperation in the field. This work was tocompatibility in animals, are often under the supported by NSF Doctoral Dissertation Improvement control of highly polymorphic genetic systems, cific individuals are mediated by precise self- Grant DEB-8I-136I7 to J. Neigel and J. Avise, and which effectively provide each sexually derived recognition systems4-7'29. Furthermore, the NSF Grant DEB-8O-22I35 to J. Avise. Contribution individual and its clonal descendants in the resolving power of a self-recognition system, No. 251 from the Discovery Bay Marine Laboratory, 2 18 23 26 University of the West Indies. population with a unique label ' - ' . The which is presumably a function of inter-clonal © 1983, American Genetic Association. possibility of using self-recognition phenom- genetic differences, may vary among popula- 134 tions. It is therefore necessary to test a self- recognition assay in the population in which it is being applied before making a definitive evaluation of its results. Recently we suggested a protocol for testing any self-recognition bioassay of clonal identity30. For a true self- recognition phenomenon that distinguishes among clonal genotypes, it is predicted that specific operational properties must charac- terize the behavior of the phenomenon with ' respect to genetic relationships: individuals should be capable of responding selectively to specific contacts; interactions between parts of the same individual or between members of the same clone should always elicit self re- FIGURE 3 Iotrochota birotulata at the EBR site. This individual is attached to a non-living coral head, sponses; interactions with different clones FIGURE 1 Verongia longissima at the WFR site of Discovery Bay. The runners of this individual are and is isolated from other areas of suitable substrate should always be responded to as non-self; extended over a coral head. by sand. responses should be reproducible; and rela- tionships defined by self responses should be transitive. These operational properties were demonstrated for naturally occurring and bioassay approach to population structure rubble. Some individuals appeared to be ac- experimental histocompatibility contact re- analysis. tively spreading over the substratum, with sponses in populations of the reef-building their encrusting bases and branches inter- t coral Acropora cervicornis. The histocompa- connected by runners (Figure 1). Smaller Materials and Methods tibility bioassay was then used to describe specimens possessed few or no branches. Our clonal structure in Acropora*0. The field work was conducted at the Dis- study site for this species was on the West Fore covery Bay Marine Laboratory of the Uni- Reef (WFR) of Discovery Bay, at a depth of In the present study we have extended the versity of the West Indies, Jamaica in March about 15 m (Figure 2). Kaye and Ortiz25 have use of histocompatibility analysis of clonal and April 1982. The two species of sponge previously shown, for a Barbados population population structure to the most primitive studied are both common on Carribean coral of this species, that both "acceptance" and invertebrate phylum, the sponges (Porifera). reefs at depths less than 20 meters. Verongia "rejection" responses could be obtained in Certain biological characteristics of sponges, longissima (Carter) was found in Jamaica on grafts between individuals. which they share with many other sessile hard substrata in non-cryptic reef locations. Iotrochota birotulata (Higgin), like V. marine invertebrates, make them especially The typical growth form was a set of several longissima, also is found on hard substratum well suited for histocompatibility analysis. branches about lem in diameter, repent or in open areas, except that it is generally con- Vegetative propagation is widespread in erect, and originating from an encrusting base fined to more solid coral heads or patch reefs; sponges, presumably because of their primitive attached to either a coral head or loose coral it is not found on loose rubble or sand. The organization and regenerative capabilities. typical growth form was a bushy clump of > Sexual reproduction in most sponges involves erect or sprawling branches of lem to 10 cm the production of motile larvae, which settle thickness (Figure 3). This species was studied on suitable substrata, metamorphose into ju- at two sites in Discovery Bay: on the West veniles and become morphologically indis- Fore Reef, in the same locale where V. long- tinguishable from vegetatively derived indi- issima was studied, and at an East Back Reef viduals3. Clones in sponge populations there- (EBR) site where a dense population was fore are initiated by larval recruitment and found in water 2-10 m deep (Figure 2). spread within the habitat by vegetative prop- The question of what the term "individual" agation. Finally, although sponges are char- should refer to when considering colonial an- acterized by a primitive cellular level of or- imals has long been deliberated27, and is ganization, some have been reported to possess especially acute in the case of sponges, where a capacity for precise self vs. non-self dis- the usual structural criteria for the individual crimination that outwardly resembles verte- units of colonial organization are inappro- > brate histocompatibility19'25. priate10. Here we will follow the usage of In this paper we will 1) consider the opera- Hartman and Reiswig16, which avoids much tional properties exhibited by histocompati- of this ambiguity, and consider "entire con- bility responses in populations of two marine fluent specimens" as individuals. demospongia, Verongia longissima and Io- Grafting experiments were
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